Introduction

It is well established that high-salt (1 g salt=0.4 g sodium) intake is the major cause of raised blood pressure and accordingly leads to cardiovascular diseases.^1,2 Recently, several lines of evidence have also shown that high salt intake is associated with an increased risk of obesity. One reason for this association is that high salt intake stimulates thirst and increases fluid intake³ and thereby increasing sugar-sweetened beverage consumption.^4,5 It has been shown that 1-g/d increase in salt intake is associated with an increase in sugar-sweetened soft drink consumption of 27 g/d in children and adolescents.⁴ The association between salt and obesity may also be partially caused by excessive consumption of processed food that is high in both calorie and salt. However, increasing evidence suggests that there may be a direct link between salt intake and obesity independent of total energy intake.^6–11 Among these studies, some used dietary method,^6,9 which is unreliable in estimating salt intake.¹² Among others who measured salt intake by the most accurate method, that is, 24-hour urinary sodium¹² and also accounted for energy intake, few assessed misreporting, especially underreporting of energy intake, which is highly prevalent¹³ particularly in overweight and obese individuals.¹⁴ Our study aimed to determine whether there was a direct association between salt intake (assessed by 24-hour urinary sodium, 24hUNa) and obesity independent of energy intake taking into account potential diet misreporting in both children and adults.

Subjects and Methods

A detailed description of the Methods is provided in the Data Supplement. The abridged methods are given below.

We used the data from the National Diet and Nutrition Survey rolling program (NDNS RP) years 1 to 4 (2008/09–2011/12). We obtained the data from the UK Data Service.¹⁵ The NDNS RP was a rolling cross-sectional study aiming to assess the nutritional status of the general UK population aged ≥1.5 years using a 4-day diary. In total, 1982 children and 2174 adults participated in the NDNS RP core survey. Among them, 458 children (age, ≥4 years) and 785 adults had valid weight and height measurement as well as complete 24-hour urine collection mainly verified by para-aminobenzoic acid¹⁶ and were included in our primary analysis. Our secondary analysis included 67 children and 117 adults who had complete 24-hour urine collection and also participated in the Doubly Labeled Water (DLW) substudy. DLW¹⁷ is the most accurate method to measure energy expenditure in free-living individuals¹⁸ and can also provide body fat mass and lean mass.

Height and weight were measured in all participants. Waist circumference was measured in individuals aged ≥11 years. Overweight and obesity was defined as body mass index (BMI) ≥85th (overweight)/95th (obese) centile according to the UK90 reference in children¹⁹ and BMI≥25 (overweight)/30(obese) in adults.²⁰ Central obesity was defined as waist circumference >102 cm for men and >88 cm for women.²⁰ In children, central obesity was defined as waist circumference at or above the age- and sex-specific 90th centile according to the International Diabetes Federation recommendation.²¹

Dietary misreporting was assessed using 2 methods. First, we compared dietary energy intake (EI_rep)/basal metabolic rate to the age- and sex-specific Goldberg cutoffs²² and classified dietary data into either plausible reports or misreports (underreport and overreport were combined as only 2 individuals were identified as overreporters). Second, we used energy expenditure derived from DLW study as a more accurate measure of total energy intake²³ in our secondary analysis.

Statistical Analysis

Our primary analysis was to explore the relationship between salt intake measured by 24hUNa and weight status. General linear models were used to obtain the adjusted mean BMI and waist circumference across the tertiles of salt intake. Logistic models were performed to identify the association of salt intake with the risk of overweight/obese and central obesity. In multivariate models, we adjusted for age, sex, ethnic group, household income, physical activity, energy intake, and misreporting (1=misreporting, 0=plausible report)^24,25 and in adults with additional adjustment of alcohol consumption, smoking, and education level (model-a). Energy intake was replaced with sugar-sweetened beverages in the second model (model-b). Furthermore, to reduce potential bias caused by residual confounding, we calculated the propensity score²⁶ of salt intake, which is the conditional probability of consuming higher salt intake, based on all confounders in model-a, and sugar-sweetened beverage consumption. Salt intake and the propensity score of higher salt intake were included in model-c. To further control energy intake, we performed a separate analysis replacing salt and energy intake in model-a with the ratio of salt/energy intake (g/2000 kcal; model-d). Logistic regression on central obesity was not performed for children because the sample size of central obesity in children was small.

Our secondary analysis aimed to examine the association between salt intake measured by 24hUNa and body composition (body lean mass and fat mass) measured by DLW. We used general linear models with adjustment for age, sex, ethnic group, and total energy intake. We also performed a separate analysis using the ratio of salt/total energy intake.

We performed several sensitivity analyses to test the robustness of the results. First, we replaced salt intake measured by 24hUNa with salt intake calculated from the 4-day diary. Second, we excluded individuals who potentially misreported their dietary intakes.

We also performed an additional analysis to explore the association between potassium and obesity using the same methods as for salt, the results of which are provided in the Data Supplement.

Results

Table 1 shows the characteristics of the study population according to tertiles of salt intake for children and adults. The mean salt intake as measured by 24hUNa was 5.5±2.7 (SD) g/d in children and 7.6±3.3 g/d in adults. Compared with the participants in the lowest salt intake tertile, those who consumed more salt tended to be men, older children, younger adults, have more energy intake, and have larger BMI and waist circumference. Children who had higher salt intake had slightly less physical exercise.

Association Between Salt Intake Measured by 24hUNa and Continuous Measurement of Weight Status

As illustrated in Figure, both BMI and waist circumference increased from the lowest to the highest tertile of salt intake (both P for trend<0.001) after adjusting for age, sex, ethnic group, household income, physical activity, total energy intake, and misreporting in children. A similar trend was also observed in adults with additional adjustment for alcohol consumption, smoking, and education level.

• Download figure
• Download PowerPoint

Association Between Salt Intake Measured by 24hUNa and Obesity Risk

Table 2 shows the relationship between salt intake and weight status. In children, a 1-g/d increase in salt intake was associated with a 28% increase in the risk of overweight or obesity (odds ratio [OR], 1.28; 95% confidence interval [CI], 1.12–1.45) after adjusting for age, sex, ethnic group, household income, physical activity, total energy intake, and misreporting (model-a). The association was almost identical when total energy intake was replaced with the consumption of sugar-sweetened beverages in model-b (OR, 1.28; 95% CI, 1.12–1.47) or replacing all the confounding factors with the propensity score of higher salt intake in model-c (OR, 1.27; 95% CI, 1.11–1.44; Table 2).

In adults, a 1-g/d increase in salt intake was associated with an increase in the risk of overweight or obesity by 26% (OR, 1.26; 95% CI, 1.16–1.37) in model-a. This figure increased to 28% (OR, 1.28; 95% CI, 1.17–1.39) when total energy intake was replaced with the consumption of sugar-sweetened beverages (model-b) but decreased to 21% (OR, 1.21; 95% CI, 1.13–1.31) when replacing all the potential confounding factors with the calculated propensity score of higher salt intake (model-c). Higher salt intake was also associated with an increase in the risk of central obesity by ≈20% in adults in all 3 models (Table 2).

Further analysis showed that a higher salt/energy ratio was also significantly associated with an increased risk of obesity in both children and adults in model-d (Table 2).

Association Between Salt Intake Measured by 24hUNa and Body Composition

As shown in Table 3, a 1-g/d increase in salt intake was associated with an increase of 0.73 kg (P=0.001) and 0.44 kg (P=0.033) in body fat mass and lean mass, respectively, in children after adjusting for age, sex and ethnic group, and energy intake. In adults, a 1-g/d increase in salt intake was associated with an increase of 0.91 kg (P=0.001) and 0.32 kg (P=0.054) in body fat mass and lean mass, respectively. A separate analysis replacing salt and energy intake with the ratio of salt/energy showed a significant association between salt intake and body fat mass (P<0.05), but the association between salt intake and body lean mass disappeared in both children and adults (Table 3).

Association Between Salt Intake Estimated From Dietary Record and Obesity Risk

In total, 1531 children (age ≥4 years) and 1991 adults completed the dietary record and were included in this sensitivity analysis. As shown in Table 4, there was a consistent significant association between dietary salt intake and weight status after adjusting for the same confounding factors as the primary analysis in model-a, model-b, and model-d in children, and the results were similar to those in the primary analysis. In adults, the corresponding association became weaker than that found in the primary analysis but was still significant in all analyses for model-a and model-b except for the association with overweight or obese which was borderline significant in model-a (P=0.06). These results were not surprising considering that under-reporting was more prevalent in adults (≈56%) compared with children (≈33%). As salt intake estimated from dietary data always had the issue of misreporting, propensity score may further introduce misclassification bias. The analysis using this index (model-c) was therefore not performed.

A separate analysis by excluding individuals who had misreported dietary energy intakes showed consistently significant and similar results as those from the primary analysis (Table 2) but with a wider confidence interval (Table S1 in the Data supplement).

Discussion

Our study was the first to have explored the association between salt intake measured by 24-hour urinary sodium and obesity in a national representative sample of the UK population. Energy intake was accounted for with critical assessment of diet misreporting. The results showed a consistent significant association between salt intake and various measures of adiposity, including BMI, waist circumference, and body fat mass, after adjusting for potential confounding factors, including total energy intake and sugar-sweetened beverage consumption. These findings suggest a direct association between salt intake and obesity independent of energy intake.

Our findings are consistent with the main body of evidence in this area. Several previous studies showed that salt intake was positively related to weight status^6–11,27,28 and the significant association persisted after adjusting for energy intake^6–11 despite there were methodological problems, such as inaccurate measurement of salt intake^6,9,10 and uncontrolled misreporting of energy intake.

Strengths and Limitations

Our study has several strengths. First, the participants were a national representative sample of the UK population including both children and adults. Second, we used salt intake measured by complete 24-hour urinary sodium excretion mainly verified by para-aminobenzoic acid, which is the most accurate method for assessing salt intake.¹² We further tested the robustness of the results in the sensitivity analysis using salt intake estimated from a 4-day food diary. Third, we assessed the misreporting of dietary energy intake and adjusted for energy intake using different methods. (1) We adjusted for misreporting as a confounder in the primary analysis and further accounted for it by excluding misreports in the sensitivity analysis. (2) We controlled for energy intake by including it as an independent variable or using the ratio of salt/energy intake in different models. These analyses revealed a consistent association between salt intake and obesity independent of energy intake. Finally, we calculated the cutoffs for misreporting using the data derived from the DLW substudy. DLW is the gold-standard method for assessing energy intake,¹⁸ but because of high cost it is hardly used in population-based studies. NDNS RP is one of the few surveys that included DLW method and therefore provided valuable data for us to validate dietary energy intake and to explore the association between salt intake and body composition.

Our study also has several limitations. As a cross-sectional study, the results derived from our study cannot draw a causal relationship between salt intake and obesity. Although our study, in conjunction with other evidence from experimental, cross-sectional as well as prospective cohort studies, indicates that high salt intake is likely to be a contributing factor for obesity, we cannot exclude the possibility that adiposity may predispose people to a higher salt consumption independent of energy intake. Furthermore, 24-hour urine and waist circumference were measured in the second stage of the NDNS RP and there was about 2 to 4 months gap between the first and second stage of the survey. However, because of labor and practical circumstance, this was inevitable in large-scale surveys and the robustness of the results were also tested using salt intake estimated from dietary record which was completed in the same stage as height and weight measurement.

Potential Mechanisms Whereby Salt Is Linked to Obesity

Previous studies have shown that salt intake is associated with obesity through energy intake such as increasing the consumption of sugar-sweetened beverages^4,5 and the coexistence of high salt and energy-dense junk food in diet with poor quality.²⁹ Our study along with several others suggests that high salt could possibly contribute to obesity independent of energy intake or sugar-sweetened soft drink consumption. The mechanism for such a direct link is not clear. One possible mechanism is that if more salt is eaten, this increases the volume of extracellular water which will give rise to a small increase in weight of <1 kg.³⁰ As shown in several randomized controlled trials, high salt intake could increase body weight in the short term.^31,32 Another mechanism is that salt could directly increase body fat. One experimental study showed that rats in high-salt group had a higher level of plasma leptin concentration as well as excessive accumulation of white adipose fat compared with the rats with lower salt intake.³³ Similar results were observed in epidemiological studies. A cross-sectional study conducted in adolescents revealed a positive relationship between dietary salt intake and subcutaneous abdominal adipose tissue, as well as leptin independent of energy intake.⁶ Prospective cohort studies in adolescents⁸ and adults¹¹ showed that baseline salt intake was positively associated with an increase in percentage body fat independent of energy intake. In other words, higher salt intake seems to result in greater deposition of fat suggesting that in some way salt alters body fat metabolism.

Perspectives

Our study using a national representative sample of both children and adults in the UK population showed a significant association between salt intake and various measures of adiposity independent of energy intake or sugar-sweetened beverage consumption. Although the mechanism whereby salt intake is directly related to obesity remains unclear, our findings could potentially have important public health implications. It is well established that a reduction in salt intake lowers blood pressure. Our study, in conjunction with other evidence, demonstrates that salt reduction could also reduce obesity risk. Both decreased blood pressure and obesity will reduce cardiovascular disease.

Acknowledgments

We thank the original data creators, depositors, copyright holders, the funders of the Data Collections, and the UK Data Archive for the use of data from National Diet and Nutrition Survey years 1 to 4, 2008/2009 to 2011/2012. The original data creators, depositors, or copyright holders bear no responsibility for the current analysis or interpretation.

Footnotes